The cortisol awakening response (CAR) across the female menstrual cycle

Psychoneuroendocrinology

Volumn 36, Issue 6, 2011, Pages 905-912

  Wolfram, Maren ^a   Bellingrath, Silja ^a,b   Kudielka, Brigitte M ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Ambulatory assessment; Chromatographic ovulation test; Cortisol awakening response (CAR); Estrogen; Female menstrual cycle; Gonadal steroids; Hypothalamus pituitary adrenal (HPA) axis; Hypothalamus pituitary gonadal (HPG) axis; Ovulation; Salivary cortisol

Indexed keywords

HYDROCORTISONE;

ADULT; ANALYSIS OF VARIANCE; ANALYTICAL EQUIPMENT; AROUSAL; ARTICLE; CONTROLLED STUDY; CORTISOL AWAKENING RESPONSE; EMOTIONALITY; FEMALE; FOLLICULAR PHASE; HORMONE RESPONSE; HUMAN; HUMAN EXPERIMENT; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LUTEAL PHASE; MENSTRUAL CYCLE; NORMAL HUMAN; OVULATION; PRIORITY JOURNAL; SALIVA ANALYSIS; SLEEP; STUDENT;

AFFECT; CIRCADIAN RHYTHM; EMOTIONS; ESTRADIOL; FEMALE; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LUTEINIZING HORMONE; MENSTRUAL CYCLE; OVULATION; PITUITARY-ADRENAL SYSTEM; PROGESTERONE; REFERENCE VALUES; SALIVA; SLEEP; WAKEFULNESS;

EID: 79956291305     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2010.12.006     Document Type: Article

References (70)

1. Abizaid A., Mezei G., Horvath T.L. Estradiol enhances light-induced expression of transcription factors in the SCN. Brain Res. 2004, 1010:35-44.
2. Abplanalp J.M., Livingston L., Rose R.M., Sandwisch D. Cortisol and growth hormone responses to psychological stress during the menstrual cycle. Psychosom. Med. 1977, 39:158-177.
3. Adam E.K., Hawkley L.C., Kudielka B.M., Cacioppo J.T. Day-to-day dynamics of experience-cortisol associations in a population-based sample of older adults. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17058-17063.
4. Altemus M., Redwine L., Leong Y.M., Yoshikawa T., Yehuda R., Detera-Wadleigh S., Murphy D.L. Reduced sensitivity to glucocorticoid feedback and reduced glucocorticoid receptor mRNA expression in the luteal phase of the menstrual cycle. Neuropsychopharmacology 1997, 17:100-109.
5. Altemus M., Roca C., Galliven E., Romanos C., Deuster P. Increased vasopressin and adrenocorticotropin responses to stress in the midluteal phase of the menstrual cycle. J. Clin. Endocrinol. Metab. 2001, 86:2525-2530.
6. Badrick E., Kirschbaum C., Kumari M. The relationship between smoking status and cortisol secretion. J. Clin. Endocrinol. Metab. 2007, 92:819-824.
7. Bao A.M., Liu R.Y., Van Someren E.J., Hofman M.A., Zhou J.N. Changes in diurnal rhythms of free cortisol secretion during different phases of menstrual cycle. Acta Physiol. Sin. 2003, 55:547-553.
8. Biehl B., Dangel S., Reiser A. Profile of mood states. Collegium Internationale Psychiatriae Scalarum 1986, Weinheim, Beltz.
9. Bloch M., Schmidt P.J., Su T.P., Tobin M.B., Rubinow D.R. Pituitary-adrenal hormones and testosterone across the menstrual cycle in women with premenstrual syndrome and controls. Biol. Psychiatry 1998, 43:897-903.
10. Bossmar T., Forsling M., Akerlund M. Circulating oxytocin and vasopressin is influenced by ovarian steroid replacement in women. Acta Obstet. Gynecol. Scand. 1995, 74:544-548.
11. Bouma E.M., Riese H., Ormel J., Verhulst F.C., Oldehinkel A.J. Adolescents' cortisol responses to awakening and social stress; effects of gender, menstrual phase and oral contraceptives. The TRAILS study. Psychoneuroendocrinology 2009, 34:884-893.
12. Buijs R.M., van Eden C.G., Goncharuk V.D., Kalsbeek A. The biological clock tunes the organs of the body: timing by hormones and the autonomic nervous system. J. Endocrinol. 2003, 177:17-26.
13. Buijs R.M., Wortel J., Van Heerikhuize J.J., Kalsbeek A. Novel environment induced inhibition of corticosterone secretion: physiological evidence for a suprachiasmatic nucleus mediated neuronal hypothalamo-adrenal cortex pathway. Brain Res. 1997, 758:229-236.
14. Burgess L.H., Handa R.J. Chronic estrogen-induced alterations in adrenocorticotropin and corticosterone secretion, and glucocorticoid receptor-mediated functions in female rats. Endocrinology 1992, 131:1261-1269.
15. Burgess L.H., Handa R.J. Estrogen-induced alterations in the regulation of mineralocorticoid and glucocorticoid receptor messenger RNA expression in the female rat anterior pituitary gland and brain. Mol. Cell Neurosci. 1993, 4:191-198.
16. Calogero A.E., Gallucci W.T., Gold P.W., Chrousos G.P. Multiple feedback regulatory loops upon rat hypothalamic corticotropin-releasing hormone secretion. Potential clinical implications. J. Clin. Invest. 1988, 82:767-774.
17. Carandente F., Angeli A., Candiani G.B., Crosignani P.G., Dammacco F., De Cecco L., Marrama P., Massobrio M., Martini L. Rhythms in the ovulatory cycle. 3rd. Cortisol and dehydroepiandrosterone sulphate (DHEA-S). Chronobiologia 1990, 17:209-217.
18. Carey M.P., Deterd C.H., de Koning J., Helmerhorst F., de Kloet E.R. The influence of ovarian steroids on hypothalamic-pituitary-adrenal regulation in the female rat. J. Endocrinol. 1995, 144:311-321.
19. Chida Y., Steptoe A. Cortisol awakening response and psychosocial factors: a systematic review and meta-analysis. Biol. Psychol. 2009, 80:265-278.
20. Clow A., Hucklebridge F., Stalder T., Evans P., Thorn L. The cortisol awakening response: more than a measure of HPA axis function. Neurosci. Biobehav. Rev. 2010, 35:97-103.
21. Clow A., Thorn L., Evans P., Hucklebridge F. The awakening cortisol response: methodological issues and significance. Stress 2004, 7:29-37.
22. Collins A., Eneroth P., Landgren B.M. Psychoneuroendocrine stress responses and mood as related to the menstrual cycle. Psychosom. Med. 1985, 47:512-527.
23. Desantis A.S., Adam E.K., Mendelsohn K.A., Doane L.D. Concordance between self-reported and objective wakeup times in ambulatory salivary cortisol research. Int. J. Behav. Med. 2010, 17:74-78.
24. Feldman S., Weidenfeld J. Depletion of hypothalamic norepinephrine and serotonin enhances the dexamethasone negative feedback effect on adrenocortical secretion. Psychoneuroendocrinology 1991, 16:397-405.
25. Fries E., Dettenborn L., Kirschbaum C. The cortisol awakening response (CAR): facts and future directions. Int. J. Psychophysiol. 2009, 72:67-73.
26. Galliven E.A., Singh A., Michelson D., Bina S., Gold P.W., Deuster P.A. Hormonal and metabolic responses to exercise across time of day and menstrual cycle phase. J. Appl. Physiol. 1997, 83:1822-1831.
27. Genazzani A.R., Lemarchand-Beraud T., Aubert M.L., Felber J.P. Pattern of plasma ACTH, hGH, and cortisol during menstrual cycle. J. Clin. Endocrinol. Metab. 1975, 41:431-437.
28. Heitkemper M., Jarrett M., Bond E.F., Turner P. GI symptoms, function, and psychophysiological arousal in dysmenorrheic women. Nurs. Res. 1991, 40:20-26.
29. Hellhammer J., Fries E., Schweisthal O.W., Schlotz W., Stone A.A., Hagemann D. Several daily measurements are necessary to reliably assess the cortisol rise after awakening: state- and trait components. Psychoneuroendocrinology 2007, 32:80-86.
30. Kanaley J.A., Boileau R.A., Bahr J.M., Misner J.E., Nelson R.A. Cortisol levels during prolonged exercise: the influence of menstrual phase and menstrual status. Int. J. Sports Med. 1992, 13:332-336.
31. Kerdelhue B., Brown S., Lenoir V., Queenan J.T., Jones G.S., Scholler R., Jones H.W. Timing of initiation of the preovulatory luteinizing hormone surge and its relationship with the circadian cortisol rhythm in the human. Neuroendocrinology 2002, 75:158-163.
32. Kiesner J., Pastore M. Day-to-day co-variations of psychological and physical symptoms of the menstrual cycle: Insights to individual differences in steroid reactivity. Psychoneuroendocrinology 2010, 35:350-363.
33. Kirschbaum C., Kudielka B.M., Gaab J., Schommer N.C., Hellhammer D.H. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom. Med. 1999, 61:154-162.
34. Kirschbaum C., Schommer N., Federenko I., Gaab J., Neumann O., Oellers M., Rohleder N., Untiedt A., Hanker J., Pirke K.M., Hellhammer D.H. Short-term estradiol treatment enhances pituitary-adrenal axis and sympathetic responses to psychosocial stress in healthy young men. J. Clin. Endocrinol. Metab. 1996, 81:3639-3643.
35. Kruyt N., Rolland R. Cortisol, 17 alpha-OH, progesterone and androgen responses to a standardized ACTH-stimulation in different stages of the normal menstrual cycle. Acta Endocrinol. (Copenh) 1982, 100:427-433.
36. Kudielka B.M., Broderick J.E., Kirschbaum C. Compliance with saliva sampling protocols: electronic monitoring reveals invalid cortisol daytime profiles in noncompliant subjects. Psychosom. Med. 2003, 65:313-319.
37. Kudielka B.M., Federenko I.S., Hellhammer D.H., Wüst S. Morningness and eveningness: the free cortisol rise after awakening in early birds and night owls. Biol. Psychol. 2006, 72:141-146.
38. Kudielka B.M., Hawkley L.C., Adam E.K., Cacioppo J.T. Compliance with ambulatory saliva sampling in the Chicago health, aging, and social relations study and associations with social support. Ann. Behav. Med. 2007, 34:209-216.
39. Kudielka B.M., Hellhammer D.H., Wüst S. Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge. Psychoneuroendocrinology 2009, 34:2-18.
40. Kudielka B.M., Hellhammer J., Hellhammer D.H., Wolf O.T., Pirke K.M., Varadi E., Pilz J., Kirschbaum C. Sex differences in endocrine and psychological responses to psychosocial stress in healthy elderly subjects and the impact of a 2-week dehydroepiandrosterone treatment. J. Clin. Endocrinol. Metab. 1998, 83:1756-1761.
41. Kudielka B.M., Kirschbaum C. Awakening cortisol responses are influenced by health status and awakening time but not by menstrual cycle phase. Psychoneuroendocrinology 2003, 28:35-47.
42. Kudielka B.M., Schmidt-Reinwald A.K., Hellhammer D.H., Kirschbaum C. Psychological and endocrine responses to psychosocial stress and dexamethasone/corticotropin-releasing hormone in healthy postmenopausal women and young controls: the impact of age and a two-week estradiol treatment. Neuroendocrinology 1999, 70:422-430.
43. Kudielka B.M., Wüst S. Human models in acute and chronic stress: assessing determinants of individual hypothalamus-pituitary-adrenal axis activity and reactivity. Stress 2010, 13:1-14.
44. Kudielka B.M., Wüst S. The cortisol awakening response (CAR): a useful tool for ambulant assessment of hypothalamus-pituitary-adrenal (HPA) axis activity. Progress in Circadian Rhythm Research 2008, 223-234. New York, Nova Science Publishers, Inc. A.-L. Léglise (Ed.).
45. Leibenluft E., Fiero P.L., Rubinow D.R. Effects of the menstrual cycle on dependent variables in mood disorder research. Arch. Gen. Psychiatry 1994, 51:761-781.
46. Maccari S., Mormede P., Piazza P.V., Simon H., Angelucci L., Le Moal M. Hippocampal type I and type II corticosteroid receptors are modulated by central noradrenergic systems. Psychoneuroendocrinology 1992, 17:103-112.
47. Marinari K.T., Leshner A.I., Doyle M.P. Menstrual cycle status and adrenocortical reactivity to psychological stress. Psychoneuroendocrinology 1976, 1:213-218.
48. McEwen B.S. Steroid hormone actions on the brain: when is the genome involved?. Horm. Behav. 1994, 28:396-405.
49. McNair D.M., Lorr M., Doppleman L.F. Manual for the Profile of Mood States 1971, Educational and Industrial Testing Services, San Diego.
50. Odber J., Cawood E.H., Bancroft J. Salivary cortisol in women with and without perimenstrual mood changes. J. Psychosom. Res. 1998, 45:557-568.
51. Okun M.L., Krafty R.T., Buysse D.J., Monk T.H., Reynolds C.F., Begley A., Hall M. What constitutes too long of a delay? Determining the cortisol awakening response (CAR) using self-report and PSG-assessed wake time. Psychoneuroendocrinology 2010, 35:460-468.
52. Ossewaarde L., Hermans E.J., van Wingen G.A., Kooijman S.C., Johansson I.M., Backstrom T., Fernandez G. Neural mechanisms underlying changes in stress-sensitivity across the menstrual cycle. Psychoneuroendocrinology 2010, 35:460-468.
53. Parker C.R., Winkel C.A., Rush A.J., Porter J.C., MacDonald P.C. Plasma concentrations of 11-deoxycorticosterone in women during the menstrual cycle. Obstet. Gynecol. 1981, 58:26-30.
54. Parry B.L., Javeed S., Laughlin G.A., Hauger R., Clopton P. Cortisol circadian rhythms during the menstrual cycle and with sleep deprivation in premenstrual dysphoric disorder and normal control subjects. Biol. Psychiatry 2000, 48:920-931.
55. Pfaff D.W., McEwen B.S. Actions of estrogens and progestins on nerve cells. Science 1983, 219:808-814.
56. Pruessner J.C., Wolf O.T., Hellhammer D.H., Buske-Kirschbaum A., von Auer K., Jobst S., Kaspers F., Kirschbaum C. Free cortisol levels after awakening: a reliable biological marker for the assessment of adrenocortical activity. Life Sci. 1997, 61:2539-2549.
57. Rubinow D.R., Hoban M.C., Grover G.N., Galloway D.S., Roy-Byrne P., Andersen R., Merriam G.R. Changes in plasma hormones across the menstrual cycle in patients with menstrually related mood disorder and in control subjects. Am. J. Obstet. Gynecol. 1988, 158:5-11.
58. Scheer F.A., Buijs R.M. Light affects morning salivary cortisol in humans. J. Clin. Endocrinol. Metab. 1999, 84:3395-3398.
59. Schmidt-Reinwald A., Pruessner J.C., Hellhammer D.H., Federenko I., Rohleder N., Schurmeyer T.H., Kirschbaum C. The cortisol response to awakening in relation to different challenge tests and a 12-hour cortisol rhythm. Life Sci. 1999, 64:1653-1660.
60. Stalder T., Hucklebridge F., Evans P., Clow A. Use of a single case study design to examine state variation in the cortisol awakening response: relationship with time of awakening. Psychoneuroendocrinology 2009, 34:607-614.
61. Steiner M., Macdougall M., Brown E. The premenstrual symptoms screening tool (PSST) for clinicians. Arch. Womens Ment. Health 2003, 6:203-209.
62. Tersman Z., Collins A., Eneroth P. Cardiovascular responses to psychological and physiological stressors during the menstrual cycle. Psychosom. Med. 1991, 53:185-197.
63. Turner B.B. Influence of gonadal steroids on brain corticosteroid receptors: a minireview. Neurochem. Res. 1997, 22:1375-1385.
64. Vamvakopoulos N.C., Chrousos G.P. Evidence of direct estrogenic regulation of human corticotropin-releasing hormone gene expression. Potential implications for the sexual dimophism of the stress response and immune/inflammatory reaction. J. Clin. Invest. 1993, 92:1896-1902.
65. Viau V. Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. J. Neuroendocrinol. 2002, 14:506-513.
66. Viau V., Meaney M.J. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991, 129:2503-2511.
67. Wilhelm I., Born J., Kudielka B.M., Schlotz W., Wüst S. Is the cortisol awakening rise a response to awakening?. Psychoneuroendocrinology 2007, 32:358-366.
68. Wong M., Moss R.L. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J. Neurosci. 1992, 12:3217-3225.
69. Wüst S., Federenko I., Hellhammer D.H., Kirschbaum C. Genetic factors, perceived chronic stress, and the free cortisol response to awakening. Psychoneuroendocrinology 2000, 25:707-720.
70. Wüst S., Wolf J., Hellhammer D.H., Federenko I., Schommer N., Kirschbaum C. The cortisol awakening response-normal values and confounds. Noise Health 2000, 2:79-88.